Neural circuits in the mouse retina support color vision in the upper visual field

ABSTRACT Color vision is essential to the survival of most animals. Its neural basis lies in the retina, where chromatic signals from different photoreceptor types sensitive to distinct wavelengths are locally compared by neural circuits. Mice, like most mammals, are generally dichromatic and have two cone photoreceptor types. However, in the ventral retina most cones display the same spectral preference, impairing spectral comparisons necessary for color vision. This conflicts with behavioral evidence showing that mice can discriminate colors only in the corresponding upper visual field. Here, we systematically investigated the neural circuits underlying mouse color vision across three processing stages of the retina by recording the output of cones, bipolar and ganglion cells using two-photon imaging. Surprisingly, we found that across all retinal layers most color-opponent cells were located in the ventral retina. This started at the level of the cone output, where color-opponency was mediated by horizontal cells and likely involving rod photoreceptors. Next, bipolar cells relayed the chromatic information to ganglion cells in the inner retina, where type-specific, non-linear center-surround interactions resulted in specific color-opponent output channels to the brain. This suggests that neural circuits in the mouse retina are specifically tuned to extract color information from the upper visual field, aiding robust detection of aerial predators and ensuring the animal’s survival.